I THE JOURNAL OF I AVIATIONMEDICINE O&hl Publication of the Aero Medical Association I 1 VOLUME 28 AUGUST, 1957 NUMBER 4

The Labyrinthine Posture Reflex (Righting Reflex] in the Cat during

BY SIEGFRIEDJ. GERATHEWOHL,PH.D., AND MAJORHERBERT D. STALLINGS,USAF

LTHOUGH it is generally ac- inner known as organs. cepted that linear acceleration They are located in the and is the physical stimulus for the the which are filmled with endo- otolith organ, its function during per- lymph and contain the very special- iods of increased and decreased grav- ized structure of macula and . ity has not been ~larified.~,~J~In 1952, The otolith apparatus consists of a SlaterlG discussed the probable re- plaque of hair cells covered with a sponse of the otoliths to the weightless mucus layer, which carries a large condition by drawing some tentative number of very small particles of cal- conclusion from morphologic data and cium carbonate, the so-called otoliths. electrophysiologic experiments made When the head is in an upright posi- by Adrian1 and Lowensteing, and by tion, the macula of the utricle lies ap- Lowenstein and Raberts.lo The experi- proximately in a horizontal plane, that ments in this report deal with the of the saccule in a vertical plane. The otolith functions of the cat. The find- planes of the two saecular maculas ings are thought to throw some light form an angle opening forward and on the vestibular processes during sub- downward. gravity and zero-gravity. The probable response of this organ The means of sensing the effect of to weightlessness has been discussed gravity, which is actually a linear ac- elsewhere.6+ Because of their physical celerative force, is provided by a set characteristics, the otoliths are "gravi- of mechanically affected organs of the receptors." They can move within the macula under the pull of their own From the U. S. Air Force School of weight, or in response to accelerative Aviation Medicine, Randolph Air Force Base, Texas. forces and their inertial effects. This Presented on May 8, 1957 at the 28th movement bends or pulls, or shears annual meeting of the Aero Medical As- sociation, Denver, Colora'do. the epithelial hairs, thus distorting the 345 POSTURE REFLEX--GERATHEWOI-IL AND STALLINGS sensory cells and producing a stimulus. gravity has an essential effect upon Depending upon the position of the animal life. This effect is very diffi- head in the state of rest, the end cult to assess but relatively easy to org'ans of the utricle and saccule are demonstrate. affected in a certain way. The forces One of the best-known reflexes of of gravity and acceleration, caused by this sort is the postural righting reflex voluntary and involuntary motion, are of the cat. Since the pioneer work of also conveyed to the brain in the Magnus, ~2'13 this reflex has been form of impulses traveling along the studied under various conditions. If . These impulses are a cat is first held in any other than all of the same intensity but they vary normal position and then dropped, the in frequency depending upon the di- animal immediately turns into the nor- rection and mode of acceleration. mal posture so that it always lands on The weight or movement of an oto- its feet. A similar reaction occurs when lith distorts the cell or cells closest to the cat, lying on its back with its head it. Minimal stimulation occurs when held in an almost normal position, is the maculas are horizontal and the moved vertically downward. However, otoliths rest on the hair cells ; maximal this reflex does not seem to function stimulation is obtained when the oto- when the cat is moved upward. Adri- liths hang from the cells or, with nor- an's experiment on the cat has shown mal head position, when they are that .changes in head position were as- pushed upward. Now, in the weight- less state, the otoliths are deprived of sociated with an alteration of the iln- their weight, too, and this should result pulse rate, which was caused either by in a minute change of the cell struc- the act of tilting or by the angle of ture. This then will bring forth an tilt as such. He found that pressure alteration of the impulse rate of the toward the macula did not increase vestibular nerve. the stimulus. This may account for the It is the opinion of many investiga- lack of postural righting reflex during tors that the fo.rce of gravity exerts movement in the upward direction. the most fundamental influence upon From a practical viewpoint the ques- our spatial orientation. ~,7,11,14 How- tion was asked how the righting reflex ever, there is no need for the organism of the cat would work during sub- to obtain a conscious knowledge of the gravity and zero-gravity. Would the direction and amount of gravity. The cat turn around when held upside basic need is for a mechanism that d.own or would it stay in this position ? adapts the body automatically to their Is there a time factor involved which effects. This is done by means of the so-called postural reflexes which are may indicate adjustment and adapta- thought to serve to maintain or restore tion? How will other cues--for in- the "normal" position and posture of stance, visual orientation--affect the the body. This group of reflexes, functioning of the reflex? The an- which includes the static and statoklne- swers to these questions were sought tic reflexes of the body, reveals that not only to satisfy ottr own curiosity, 346 AVIATION MEDICINE POSTURE REFLEX--GERATHEWOHL AND STALLINGS bu,t to clarify the role of the otolith an altitude of approximately 12,000 organ during weightlessness. feet. The pilot of the craft (H.D.S.) flew the ascending arc of the para- METHOD bola at full throttle and the descend- Eight cats were used in the ex- ing part with about 75 per cent rpm periment; all were healthy young ani- in order to obtain weightlessness for mals born in the School of Aviation about 25 to 35 seconds. A.bsolute Medicine cat and dog kennels, and weightlessness or zero-gravity oc- raised from three different litters. curred for only a few seconds during Four of the kittens were about three each of t:hese maneuvers due to the weeks old when used in the experi- small accelerative forces present. These ment; two of the kittens were about unavoidable accelerations were of an eight weeks, and two young cats were estimated magnitude of about 0.03 to about twelve weeks of age. The ex- 0.05 G. The weightless state was indi- periments were conducted as follows: cated and controlled by the convention- Each of the three sets of experi- al G-meter installed in all fighter type mental animals first was taken into aircraft. Before entering into the para- the School of Aviation Medicine film bo.la and during recovery from the studio and placed on a table. The ani- dive, accelerations .of 1.25 G were not mals were then lifted up individually to be exceeded because it was observed and held upside-down in a long du'ring the first flight that the cats stretched position. They were released were extremely sensitive to an increase unexpectedly and dropped from an of acceleration. Five or six parabolas altitude of about 20 inches. Wfien the were performed during each experi- three-week-old kittens were employed, mental flight. the table was covered with a rubber The small kittens were taken along pad. In some of these experiments in pairs and kept in a container until the animals were blindfolded to ex- the working altitude was reached. The clude visual orientation. The behavior older animals were used one at a time of the animals was recorded on film. and carried on the arm of the experi- This experiment was repeated several menter in the aircraft (Fig. 1). The times so that its result could be con- cats were turned upside-down and re- sidered conclusive. leased after periods of 1, 51 10, 15, 20 The animals were then taken into and 25 seconds after entering the the air and exposed to short periods of weightless state. The behavior of the weightlessness. Virtual weightless- animals was studied under 'both blind- ness, or a state of reduced gravity, fold and nonblindfold conditions and was produced by flying a jet type air- recorded on film. craft (T-33 or F-94) along a Kep- Motion pictures were made using lerian trajectory. 4'5 The ascent to a 16 ram. Filmo camera, model 70 H, 20,000 feet was made at a rate of with a 13 mm. lens, f ~ 1.5, and a climb of 2,000 feet per minute. T'he film speed of 24 frames per second. cabin pressure at that altitude was Kodachrome film with a Kodak No. about 9.5 psi, which is equivalent of 83 filter, and one Eastman Panchro- Aucus~ 1957 347 POSTURE REFLEX--GERATHEWOI-'fL AND STALLINGS

Fig. 1. Photograph of Fig. 2. Prompt ,righting Fig. 3. Delayed reflex: cat before the experiment reflex of cat immediately the cat turns slowly after a in the T-33 aircraft. upon entering the weightless certain delay. condition.

9 [8 AVIATION MFA}ICINE POSTURE REFLEX--GERATHEWOFITL AND STALLINGS

Fig. 4. Postural righting Fig. 5. Disturbed reflex Fig. 6. No righting re- reflex fails completely; the associated with slight tum- flex. The animal floats cat floats in an inverted bling. slowly upwards due to ac- position. celeration in this direction (so-called "negative G").

AUGUST, 1957 349 POSTURE REFLEX--GERATHEWOFIL AND STALLINGS matic black-and-white film for illus- righting reflex of the cat develops dur- tration purposes, was used. The cam- ing the fourth tilt sixth week after era was attached to the airframe on birth. Hence, in describing the be- top of the instrument panel between havior of ou'r animals we must dis- front and rear seat of the T-33 air- tinguish between (1) the three-week- craft, and focused at a distance of old kittens whose postural righting re- about 100 can. In the F-94 aircraft flex was not developed, and (2) the the camera was installed below the eight and twelve-week-old ones whose rear panel and focused slightly upward reflex was well established. We can at a distance of about 75 cm. It was summarize the behavior of the first switched on shortly before each para- group very briefly. bola and stopped at the end of it. Some The motion pictures of the younger illustrations of the results are given kittens made on the ground and in in Figures 2, 3, 4, 5 and 6. Unfortu- the air show very clearly that in not nately, the animal is only partly visible a single case did the animals turn in these pictures because o.f the small around after they were released. They field size and the limited elevation of fell or floated in an inverted position the camera. under normal gravitational and under The evaluation of the films con- subgravitational conditions, respective- sisted of an analysis of the moving ly. Since the righting reflex was not pictures as well as the stills by de- developed, blindfolding was meaning- scribing briefly the behavior of the less, of course. The responses of this animals with regard to. promptness or group of animals were not t~bu'Iated delay .of the righting reflex under the due to the uniformity of behavior. conditions of reduced gravity. To this The behavior of the older animals, end, the films were run at normal on the other hand, showed consider- speed and additional .checks of each able differences under the various ex- scene of exposure of .the cat were perinaental conditions. On the ground, made by looking at each individual the reflex functioned promptly and so frame when the. film was moved by unanimously that the results were not hand. The observations were then tabulated either. The responses of the tabulated; the reflex response was re- four older animals upon exposure to lated to the length of time spent in weightlessness, however, were tabu- the weightless condition. Thus, some lated and are given in Tables I and I1. numerical results were obtained which In the first table, the behavior of the must be considered for what they are two eight-week-old kittens is described. worth. As can be seen in this table, the ani- mals turned .back into their normal RESULTS posture at the first exposure to weight- Even before the experiments were lessness. This reflex seems to be de- started it was observed that the four layed or disturbed in the later trials. younger animals fell straight down Table II contains the description of when they were dropped on the the two oldest animals. Again, the gen- ground. We found that the postural eral impression is that the cats turn

350 AVIATION MEDICINE POSTURE REFLEX--GERATHEWOtIL AND STALLINGS

TABLE I. BEHAVIOR OF THE ANIMAL WHEN EXPOSED IN AN UPSIDE-DOWN POSITION TO SHORT PERIODS OF WEIGHTLESSNESS AT VARIOUS INTERVALS AFTER THE SUBGRAVITY STATE BEGINS

Animal Parabola : No. of Exposure Condition Time Response Grey kitten A 1 1 Eyes open Immed. Prompt righting reflex 2 Eyes open 5 Delayed righting reflex 3 Eyes open 10 No righting but tumbling due to wild motor response 2 1 Eyes open Immed. Floating upward and delayed turninj Normal upside-down due to accelerations position acting in the opposite direction (negative g's). 3 1 Eyes open 10 No righting 2 Eyes open 15 No righting and floating upside- down for a few seconds 3 Eyes open 20 No righting reflex 4 Eyes open 25 No righting reflex 4 1 Hood 10 No righting reflex 2 Hood 15 No righting reflex 3 Eyes open 20 No righting but tumbling 4 Eyes open 25 No righting but floating 5 (?) Eyes open 30 (?) No righting, floating upward 5 1 Hood 5 No righting, floating upward 2 Hood 10 Righting, tumbling 3 Hood 15 No righting; floating upward and tumbling 3rey kitten B 1 1 Eyes open Immed. Righting reflex somewhat delayed 2 Eyes open 5 No righting, floating upward 2 1 Hood Immed. Righting, floating upward, turning again upside-down 2 Hood 10 No righting, floats upward and down- ward upside-down 3 1 Eyes open 5 Righting and turning about lon- gitudinM axis 2 Eyes open 10 Delayed righting 3 Eyes open 15 Righting reflex 4 1 Hood Immed. Righting 2 Hood 5 No righting but tumbling into ver- tical, then normal 3 Hood 10 Delayed reflex 4 Eyes open 20 Floats downward, then delayed reflex 5 1 Hood 5 Floats upward, tumbling 2 Hood 10 Floats upward, tumbling and turning in normal position 6 1 Eyes open 10 Righting 2 Eyes open 15 Delayed righting and tumbling

into the normal position during the refused to be released or clung to a first exposures; but that the reflex f.oothold in the cockpit. In column 2, is delayed or does not occur at all the given number of parabolas varies toward the end of the experiments. from five to six for the respective To obtain a clearer picture of the animal. Column 3 is subdivided in uccurrence and mode of the righting responses obtained under .blindfold reflex, particularly in regard to the and nonblindfold conditions; the first time factor, the responses of the four number being smaller because the ani- older animals were tabulated (Table mal succeeded in stripping off the hood III). In this table, the beginning of on several occasions. the exposu're of the cat t.o be weight- An inspection of Table III confirms less condition is indicated by time the observations made in the aircraft values from one to twenty-five sec- and the general impression obtained onds, which are approximations be- from Tables I and II. Upon release cause of the awkward situations which immediately, or not later than abou,t sometimes occurred when the animal 5 seconds, the animal turned into the AUGUST~ 1957 351 POSTURE REFLEX--GERATHEWOHL AND STALLINGS

TABLE II. BEHAVIOR OF THE ANIMAL WHEN EXPOSED TO SHORT PERIODS OF WEIGHTLESSNESS IN AN UPSIDE-DOWN POSITION AT VARIOUS INTERVALS AFTER THE SUBGRAVITY STATE BEGINS

Animal Parabola No. of Exposure Condition Time Response Black and white cat 1 1 Hood 5 Prompt righting reflex 2 Hood 10 Prompt rightjmg reflex 2 1 Hood 5 Prompt righting reflex 2 Hood 10 Normal position, turning upside- down due to acceleration in opposite direction (negative g's) 3 Hood 20 Delayed righting reflex and turning 1 Eyes open 10 No turning, floating upward, grasp~ top string 1 Hood Immed. Righting reflex 2 Hood 5 Righting reflex 1 Hood Immed. Righting reflex 2 Hood 5 Righting reflex 3 Hood 10 Floating, no reflex 4 Hood 15 No righting reflex 5 Hood 20 No righting reflex 1 Hood Immed. Righting reflex 2 Hood 5 Floating upward, no turning, grasp~ top string White cat l Eyes open 5 Floating upward, delayed rightinl~ reflex 1 Eyes open 5 Prompt righting reflex 2 Eyes open 10 Prompt righting reflex 3 Eyes open 15 Prompt righting reflex 1 Eyes open 5 Righting reflex 2 Eyes open 10 Floating upward, no righting 3 Eyes open 15 Floating upward, tumbling but nc righting reflex 1 Eyes open 5 Floating upward, no righting reflex 2 Eyes open 10 Floating upward, no righting reflex 3 Eyes open 15 Floating briefly, no righting reflex 1 Eyes open Immed. Righting reflex 2 Eyes open 5 Delayed righting reflex 3 Eyes open 15 Righting reflex, slightly delayed

normal position eleven times when DISCUSSION visual cues were available, and ten Magnus 12 has demonstrated that times when they were blindfolded. normal animals acqu~ire and maintain After a latency of about 15 or 20 sec- posture by various static and stato- onds, the righting reflex occurred or kinetic reactions. In our experiments, failed about the same number of times both types of reflexes will also be when tile cats were not blindfolded. activated because the cat normally does W'hen the hood was used, the same not like to lie on its ~back, nor to be ratio of responses was already ob- moved irt this position in a vertical tained after 10 seconds. From this direction. When a cat is held back time on the reflex failed in five cases. downward and then allowed to fall, With eyes open no righting response the otollth reflex acting upon the neck was observed among the few cases ex- muscles turns the head of the animal posed after a period of twenty-five rapidly into its normal position. The seconds. By and large, we found that contraction of the neck muscles, which the postural righting reflex ceased to rotate the head, activates the myotatic function after a stay of more than neck reflexes which affect the muscles twenty seconds in the weightless state; of the body by turning the thorax and and that visual .cues did not seem to then the pelvis into the normal posture. affect the reflex to a marked degree. This reaction can be seen in pictures 352 Av~TION Mv_~ICaNE POSTURE REFLEX--GERATI-IEWOI~L AND STALLINGS

TABLE III. OCCURRENCE OF RIGHTING REFLEX AT VARIOUS INTERVALS AFTER THE SUB- AND ZERO-GRAVITY STATES BEGIN

Beginning of Exposure of Animal in Seconds With Eyes Open Wit Hood Animal Parabola 1 5 10 15 20 25 1 5 I~ i [ 20 25 Grey kitten A 1 + • -- 2 x* 3 4 5

Grey kitten B 1 -F -- 2 + 3 + + + 4 + -I- -t- 5 6 -t- •

Black and white cat 21 ++x+. 3 4 5 ;++ 6 q- --

White cat 1 2 + + 3 -t- -- -- 4 5 + _+ +

Righting reflex (-l-) 6 2 3 1 1 7 3 1 Delayed reflex (4-) 1 2 1 1 2 No righting reflex (--) 3 5 2 2 2 I 4 3 3 2

*Animal was held in normal position and an acceleration opposite to the direction and stronger than the force of gravity was employed. of a promptly functioning righting re- Because visual ,cues play a promi- flex (Fig. 2). nent role for the orientation of the Although we have enough evidence cat, the occurrence of the so-called to assume that the postural righting re- ".opticM righting reflex" was controlled flex was generally produced by an by means of the hood. This reflex was otolith response, this reflex can be observed in those cases in which r reinforced by exteroceptic or visceral animal turned or stretched itself in stimulation. Because the animal was order to grasp the top or the side of symmetrically supported in our ex- the canopy. There is some evidence periments, reinforcement of the pos- from Ta,ble III that blindfolding tural righting reflex by the so-.called changed'the reflex pattern but slightly. "body righting reflex" can be neg- Natural.ly, we cannot expect the lected. However, there is the possibil- righting reflex to occur hero.re it has ity of a .certain reinforcement through been developed. After this was ac- the loss of touch and grip pressure complished, the reflex should fail only during the release of the animal. This if there is a complete lack of stimula- may account for some of the reflex tion. During the transition from the actior~s in an advanced state of weight- normal state of gravity into st~bgrav- lessness. ity, the gravireceptors are stimulated. AUGUST, 1957 353 POSTURE REFLEX--GERATHEWOI-IL AND STALLINGS

This may have cau'sed the righting that will stimulate the gravireceptors response of the animal when released again. immediately upon entering the weight- EI.ow powerful this stimulation can less state. On the other hand, if the be was demonstrated by the two ex- animal was in this state for a certain posures of the cats tO accelerations period of time and was then released, producing centrifugal forces different the reflex was delayed or failed. It from the direction and stronger than should have failed completely if true the force of gravity. The black and weightlessness were obtained. Hence, white cat tended to turn in the appar- it seems that the righting reactions ob- ent direction of gravity, but the re- served toward the end of the parabola flex was delayed and incomplete due were caused by the slight changes in to ,the almost normal position of ,the acceleration, which unfortunately oc- head. The grey kitten turned imme- curred during most of our weightless diately from the normal position up- periods. ward and landed in an inverted posi- The response pattern obtained in our tion at the top of the canopy. In this experiments must be attributed to the case, the physiologic condition was changed stimulus pattern of discrepant very similar to that when the kitten gravitational, visuM and tactile cues was dropped in the upside-down po- which caused spatial disorientation. sition. Because the Posture of the This may 'be the main reason why the head was inverted from one condition animal became so confused and fought to the other, the inertial effect on the against being exposed to the weight- otoliths is the same when the direction less condition, and why the postural of acceleration is reversed. The in- reflex was disturbed. These experi- verted righting response occurred al- ments also show that the otoliths most though visual cues were available. probably are not stimulated by accel- eration as such, but by the changes of SUM,MARY AND CONCLUSIONS acceleration. In the weightless condi- tion of our experiment the animal is Experiments on the postural right- subjected to the constant acceleration ing reflex were made using (1) four of gravity, but this force does not seem young kittens before the reflex was developed, and (2) four older kittens to activate the postural righting re- with the reflex well established. On flex. Physiologically, this is under- the ground, the animals were dropped standable ,because it is the initial in upside-down position from an alti- change of the physical state of the tude of abou't twenty inches, and later otoliths that ,produces an inertial effect in the air exposed to period,s of about to elicit the sensory stimulus indicat- twenty to thirty seconds of practical ing the alteration of the physical con- weightlessness. The reflex was stud- dition: Thereafter, the otoliths "move ied in T-33 and F-94 aircraft under along" with the maculae, and only the both blindfold and non-blindfold con- alteration of this condition by deceler- ditions. The behavior of the cats was ation brings forth the inertial effects recorded on 16 ram. film. 354 Av~T~o~ MF.mC~N~ POSTURE REFLEX--GERATHEWOI-IL AND STALL]NGS

The motion pictures were evaluated 4. GERATItEWOHL, S. J., STRUGHOLD, H., and STALLINGS, H. D. : Sensomotor by repeatedly watching the film, and performance during weightlessness: by an analysis of the individual Eye-hand coordination. J. Av. Med., 28:7, 1957. frames. On the ground, the younger 5. GERATttEWOHL, S. J. : Personal experi- animals fell straight down; the older ences during short periods of weight- lessness reported by sixteen subjects. ones turned upright immediately after Astronautica Acta, 4:204, 1956. release without exception. In the air, 6. GOUaF-ROT,L. : Loi de Weber- Fechner et variations de la pesanteur appar- the younger kittens floated upside- onto. Med. Aeronaut., 8:119, 1953. down du'ring weightlessness; the older 7. GRAYBIEL, A. : The oculogravic illu'- sion. USN. Sch. Avi~t. Med., Proj. ones turned upright at the beginning No. NM 059.01.27, December, 1951. of the weightless state, but their re- 8. HABER, H., and GERATHEWOHL, S. J. : Physics and psychophysics of weight- flex failed after several exposures. By lessness. J. Av. Med., 22:180, 1951. and large, it was observed that the 9. LOWENST~IN,O. : Symposia of the So- ciety for Experimental Biology postural righting reflex of the cat (Brit.), No. IV:N, 1950. ceased to function after a period of 10. L0WENSTEIN, O., and ROBERTS, T. D. M. : The equilibrium function of ~he about twenty seconds of practical otolith organs of Thornback Ray weightlessness; .and that the available (Raja clavate). J. Physiol., 110:392, 1949. visuM cues did not affect essentially 11. MACH, E.: Physikalische Versuche the reflex pattern. ueber den Gleichgewiehtssinn des Menschen. Sitzgsber. d. Kaiserl. Akad. d. Wissen.wh., 46:124, 1873. REFERENCES 12. MAGNUS,R.: Kaerperstdlu~g. Berlin: Springer, 1924. 1. ADRIAI,~,E. D. : Discharges from ves- 13. MAGNUS, R. : Studies in the physiol- tibular receptors in the cat. J. Phys- ogy of posture. Lancet, 211:531, 1926. iol., 101:389, 1943. I4. MANN, C. W. : Studies in space per- 2. CLARK, B., and GRAYBIEL,A. : Disorien- ception. USN Sch. Avlat. Med. tation: A cause of pilot error. USN Rep. No. t8, 1950. Sch. ,4viat. Med., Joint Proi. Rpt. 15. SIMONS, D. G. : Review of biological No. NM 001 100.9, March 1955. effects of subgravity and weightless- 3. GAUER, O., and HABER, H. : Man under ness. Jet Propulsion, 25:209 May, gravity-free conditions. 'In Ger~a~ 1955. Aviation Medicine, World War II, 16. SEATER, A. E. : Sensory perception of U. S. Government Printing Office, the weightless condition. Annual Rep. Washington: Department of the Air Brit. Interplanet. Soc. 1952, pp. 342- Force, 1951, pp. 641-644. 348.

Importance of Aircraft Sanitation

Domestic airlines today are spending more money to feed their passen- gers than they spem not many years ago to fly them. Airline catering has become a specialized trade. In compliance with good sanitation standards, galley equipment is designed to facilitate cleaning--corners are rounded, seams are tight, and parts are removable. Although the primary aim of sanitation is to prevent the spread of communicable disease, an immediate benefit in air travel is that protection of the pilots' health enhances safety. A pilot suffering from severe nausea, vomiting, headache, diarrhea, or cramps would be a hazard to the safety of his plane, its passengers, and its crew.--HEALTH ALOFT: Physidan's Bulletin, October, 1956.

AUGUST, 1957 355